Skip to main content
SpringerLink
Log in

Acidic and non-acidic endosomes in kidney epithelial cells: their role in cell-specific membrane recycling processes

  • Conference paper
Molecular and Cellular Mechanisms of H+ Transport

Part of the book series: NATO ASI Series ((volume 89))

  • 91 Accesses

Summary

Epithelial cells lining some kidney tubule segments have developed highly–specialized, yet independent systems for the rapid modulation their plasma membrane composition in response to different stimuli. In all cases, this process involves the movement of intracellular transporting vesicles that carry specific protein cargoes to and from the plasma membrane. These vesicles have transport features that differ among the various cell types, and this brief review will examine endosomes from the proximal tubule, and collecting duct intercalated principal cells, with respect to their content of two important proteins: water channels and proton pumps (H+ATPase). The endosomal content of these two proteins varies in relation to the physiological role of the epithelial cell types. Apical endosomes from the proximal tubule contain both proteins, intercalated cell endosomes contain proton pumps but not water channels, and principal cell apical endosomes contain water channels but lack functional proton pumps. This endosomal division of labour along the urinary tubule is summarized in Figure 1 and has been revealed using a combination of morphological, immunocytochemical and functional techniques.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aronson PS (1983) Mechanisms of active H+ secretion in the proximal tubule. Am. J. Physiol. 245: F647–F659

    CAS  PubMed  Google Scholar 

  • Brown D (1989) Membrane recycling and epithelial cell function. Am. J. Physiol. 256: F1–F12

    CAS  PubMed  Google Scholar 

  • Brown D (1991) Structural-functional features of vasopressin-induced water flow in the kidney collecting duct. Sem. Nephrol. 11: 478–501

    CAS  Google Scholar 

  • Brown D, Gluck S, Hartwig J (1987) Structure of the novel membrane-coating material in proton-secreting epithelial cells and identification as an H+ATPase. J. Cell Biol. 105: 1637–1648

    Article  CAS  PubMed  Google Scholar 

  • Brown D, Hirsch S, Gluck S (1988a) An H+ATPase is present hf opposite plasma membrane domains in subpopulations of kidney epithelial cells. Nature 331: 622–624

    Article  CAS  PubMed  Google Scholar 

  • Brown D, Hirsch S, Gluck S (1988b) Localization of a proton-pumping ATPase in rat kidney. J. Clin. Invest 82: 2114–2126

    Google Scholar 

  • Brown D, Orci L (1983) Vasopressin stimulates the formation of coated pits in rat kidney collecting ducts. Nature 302: 253–255

    Article  CAS  PubMed  Google Scholar 

  • Brown D, Weyer P, Orci L (1987) Non-clathrin coated vesicles are involved in endocytosis in kidney collecting duct intercalated cells. Anat. Rec. 218: 237–242

    Google Scholar 

  • Brown D, Weyer P, Orci L (1988) Vasopressin stimulates endocytosis in kidney collecting duct epithelial cells. Eur. J. Cell Biol. 46: 336–340

    Google Scholar 

  • Christensen EI (1976) Rapid protein uptake and digestion in proximal tubule lysosomes. Kidney Int 10: 301–310

    Article  CAS  PubMed  Google Scholar 

  • Fushimi K, Uchida S, Hara Y, Hirata Y, Marumo F, Sasaki S (1993) Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361: 549–552

    Article  CAS  PubMed  Google Scholar 

  • Gluck S, Cannon C, Al-Awqati Q (1982) Exocytosis regulates urinary acidification in turtle bladder by rapid insertion of H+ pumps into the luminal membrane. Proc. Natl Acad. Sci. U.S.A. 79: 4327–4331

    Google Scholar 

  • Gutmann EJ, Niles JL, McCluskey RT, Brown D (1989) Colchicine-induced redistribution of an endogenous apical membrane glycoprotein (gp 330) in kidney proximal tubule epithelium. Am. J. Physiol. 257: C397–C407

    CAS  PubMed  Google Scholar 

  • Harris HW, Zeidel ML, Hosselet C (1991a) Quantitation and topography of membrane proteins in highly water–permeable vesicles from ADH-stimulated toad bladder. Am. J. Physiol. 261: C143–C153

    CAS  PubMed  Google Scholar 

  • Harris HWJ, Strange K, Zeidel ML (1991b) Current understanding of the cellular biology and molecular structure of the antidiuretic hormone-stimulated water transport pathway. J. Clin. Invest. 88: 1–8

    Google Scholar 

  • Kerjaschki D, Noronha-Blob L, Sacktor B, Farquhar MG (1984) Microdomains of distinctive glycoprotein composition in the kidney proximal tubule brush border. J Cell Biol 98: 1505–1513

    Article  CAS  PubMed  Google Scholar 

  • Koichi Y, Satlin LM, Schwartz GJ (1992) Adaptation of rabbit cortical collecting duct tO in vitro acidification. Am. J. Physiol. 263: F749–F756

    Google Scholar 

  • Lencer WI, Brown D, Ausiello DA, Verkman AS (1990a) Endocytosis of water channels in rat kidney: cell specificity and correlation with in vivo antidiuresis. Am. J. Physiol. 259: C920–C932

    CAS  PubMed  Google Scholar 

  • Lencer WI, Verkman AS, Arnaout A, Ausiello DA, Brown D (1990b) Endocytic vesicles from renal papilla which retrieve the vasopressin-sensitive water channel do not contain a functional H+ATPase. J. Cell Biol. Ill: 379–390

    Google Scholar 

  • Madsen KM, Tisher CC (1986) Structure-function relationships along the distal nephron. Am. J. Physiol. 250: F1–F15

    CAS  Google Scholar 

  • Madsen KM, Verlander JW, J. K, Tisher CC (1991) Morphological adaptation of the collecting duct to acid-base disturbances. Kidney Int. 40 (Suppl. 33): S57–S63

    Google Scholar 

  • Nielsen S, Smith BL, Christensen EI, Knepper MA, Agre P (1993) CHIP28 water channels are localized in constitutively waterpermeable segments of the nephron. J. Cell Biol. 120: 371–383

    Article  CAS  PubMed  Google Scholar 

  • Preston GM, Agre P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28kilodaltons: member of an ancient channel family. Proc. Natl. Acad. Sci. 88: 11110–11114

    Google Scholar 

  • Rodman JS, Kerjaschki D, Merisko E, Farquhar MG (1984) Presence of an extensive clathrin coat on the apical plasmalemma of the rat kidney proximal tubule cell. J. Cell Biol. 98: 1630–1636

    Article  CAS  PubMed  Google Scholar 

  • Sabolic I, Haase W, Burkhardt G (1985) ATP-dependent H+ pumps in membrane vesicles from rat kidney cortex. Am. J. Physiol. 248: F835–F844

    CAS  PubMed  Google Scholar 

  • Sabolic I, Valenti G, Verbavatz J-M, et al. (1992a) Localization of the CHIP28 water channel in rat kidney. Am. J. Physiol. 263: C1225–C1233

    CAS  PubMed  Google Scholar 

  • Sabolic I, Wuarin F, Shi L-B, et al. (1992b) Apical endosomes isolated from kidney collecting duct principal cells lack subunits of the proton pumping ATPase. J. Cell Biol. 119: 111–122

    Article  CAS  PubMed  Google Scholar 

  • Schwartz GJ, Al-Awqati Q (1985) Carbon dioxide causes exocytosis of vesicles containing H+ pumps in isolated perfused proximal and collecting tubules. J. Clin. Invest. 75: 1638–1644

    Google Scholar 

  • Shi L-B, Brown D, Verkman AS (1990) Water, proton and urea transport in toad bladder endosomes that contain the vasopressin-sensitive water channel. J. Gen. Physiol. 95: 941–960

    Google Scholar 

  • Stetson DA, Steinmetz PR (1985) A and B types of carbonic anhydrase-rich cells in turtle bladder. Am. J. Physiol. 249: F553–F565

    CAS  PubMed  Google Scholar 

  • Strange K, Willingham MC, Handler JS, Harris HW Jr. (1988) Apical membrane endocytosis via coated pits is stimulated by removal of antidiuretic hormone from isolated, perfused rabbit cortical collecting tubule. J. Membr. Biol. 103: 17–28

    Google Scholar 

  • Verkman AS (1989) Mechanisms and regulation of water permeability in renal epithelia. Am. J. Physiol. 257: C837–C850

    CAS  PubMed  Google Scholar 

  • Verkman AS, Lencer WI, Brown D, Ausiello DA (1988) Endosomes from kidney collecting tubule cells contain the vasopressin-sensitive water channel. Nature 333: 268–269

    Article  CAS  PubMed  Google Scholar 

  • Verkman AS, Weyer P, Brown D, Ausiello DA (1989) Functional water channels are present in clathrin coated vesicles from bovine kidney but not from brain. J. Biol. Chem. 264: 20608–20613

    Google Scholar 

  • Verlander JW, Madsen KM, Tisher CC (1988) Effect of acute respiratory acidosis on two populations of intercalated cells in rat cortical collecting duct. Am. J. Physiol. 253: F1142–F1156

    Google Scholar 

  • Ye R, Shi LB, Lencer WI, Verkman AS (1989) Functional colocalization of water channels and proton pumps in endosomes from kidney proximal tubule. J. Gen. Physiol. 93: 885–902

    Google Scholar 

  • Zhang R, Skach W, Hasegawa H, Van Hoek AN, Verkman AS (1993) Cloning, functional analysis and cell localization of a kidney proximal tubule water transporter homologous to CHIP28. J. Cell Biol. 120: 359–369

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Renal Unit, Massachusetts General Hospital, Boston, MA, 02114, USA

    Dennis Brown & Ivan Sabolić

Authors
  1. Dennis Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivan Sabolić
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Physiological Sciences, University of Newcastle upon Tyne Medical School, Newcastle upon Tyne, NE2 4HH, UK

    Barry H. Hirst

Rights and permissions

Reprints and permissions

Copyright information

© 1994 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Brown, D., Sabolić, I. (1994). Acidic and non-acidic endosomes in kidney epithelial cells: their role in cell-specific membrane recycling processes. In: Hirst, B.H. (eds) Molecular and Cellular Mechanisms of H+ Transport. NATO ASI Series, vol 89. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79301-1_15

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-79301-1_15

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-79303-5

  • Online ISBN: 978-3-642-79301-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation